PREY PREFERENCE AND PREDATORY BEHAVIOR OF Aurantilaria aurantiaca (: : )

Preferência de presa e comportamento predatório de Aurantilaria aurantiaca (MOLLUSCA: GASTROPODA: Arquivos de Ciências do Mar FASCIOLARIIDAE)

Carlos Augusto Oliveira de Meirelles1,3, Helena Matthews-Cascon1,2

RESUMO

A família Fasciolariidae é formada por espécies carnívoras que usualmente predam outros gastrópodes e bivalves. Geralmente utilizam como estratégia de predação, o lascamento de concha, meio pelo qual o predador pode alcançar as partes moles da presa. Os objetivos desse trabalho foram determinar as possíveis presas de Aurantilaria aurantiaca da Praia do Pacheco (Caucaia-CE-Brasil) e a sua preferência alimentar em condições de laboratório. As presas observadas foram os gastrópodes , viridula e Stramonita brasiliensis. O experimento de preferência de presa foi executado acondicionando um predador em um aquário de 5 litros com um indivíduo de cada presa, sendo observado durante 60 dias (replicado 10 vezes). Para a determinação do tempo de manipulação da presa, um predador foi acondicionado em uma caixa plástica mergulhada em um aquário de 80 litros juntamente com uma espécie de presa, sendo anotado o tempo de predação por duas 2 horas, durante 30 dias (replicado 10 vezes para cada espécie de presa). Aurantilaria aurantiaca mostrou preferência por Stramonita brasiliensis, o qual teve o mais baixo tempo de manipulação da presa. Pisania pusio e Tegula viridula não apresentaram resultados estatisticamente significativos (p = 0.7235 e 0.2499, respectivamente). O comportamento predatório mostrou 2 estratégias: penetração direta da probóscide e sufocamento. Não houve registro de lascamento de concha. Aurantilaria aurantiaca apresentou-se como um predador generalista, onde a variação de tempo de manipulação da presa mostrou que o predador passou por um processo de aprendizagem.

Palavras-chave: Predação, Tempo de Manipulação da Presa, Mollusca, Gastropoda, Fasciolariidae, Aurantilaria aurantiaca.

ABSTRACT

Fasciolariid are predators that prey on other gastropods and bivalves. They usually break prey shell to reach its soft parts. In this study, prey species that Aurantilaria aurantiaca consumes at Pacheco Beach (Ceará State, Northeast Brazil) and its prey preference in laboratory conditions were determined. Prey species observed were Pisania pusio, Tegula viridula and Stramonita brasiliensis. Prey preference experiment was performed placing one individual of Aurantilaria aurantiaca and one individual of each prey species in a 5 liters tank. It lasted 60 days and was replicated 10 times. Handling time of predation on each prey was measured by placing one predator with one prey into separate plastic containers in an 80 liters tank. Observations were made every 2 hours over a 30-day period. Aurantilaria aurantiaca showed preference for Stramonita brasiliensis, which presented the shortest handling time. Pisania pusio and Tegula viridula didn’t show statistical significant results (p = 0.7235 e 0.2499 respectively). Aurantilaria aurantiaca presented 2 main predatory strategies: direct prey shell penetration and asphyxiating process. No damaged prey shells were observed. The predator showed a generalist predatory behavior. Prey handling time variations demonstrated that Aurantilaria aurantiaca predation act involved a training process.

Keywords: Predation, handling time, Mollusca, Gastropoda, Fasciolariidae, Aurantilaria aurantiaca.

1 Laboratório de Invertebrados Marinhos - LIMCE, Universidade Federal do Ceará, Centro de Ciências, Departamento de Biologia, bloco 909 Campus do Pici. CEP. 60455-970, Fortaleza, Ceará, Brazil.Email: [email protected] 2 Instituto de Ciências do Mar (LABOMAR), Universidade Federal do Ceará, Fortaleza, Ceará, Brazil. 3 Programa de Pós-Graduação em Engenharia de Pesca – Universidade Federal do Ceará, Fortaleza, Ceará, Brazil.

Arq. Ciên. Mar, Fortaleza, 2016, 49(2): 23 - 32 23 INTRODUCTION have been explained by OFT (Abe, 1989; Hughes & Burrows, 1993). Sih & Christensen (2001) have A predator has to make decisions about what, concluded that the OFT could explain the prey where and when to eat (Krebs, 1977). According to selection if the predator feeds on sessile species. optimal foraging theory (OFT), the feeding strategies According to Yamamoto (2004) there is not enough presented by an organism are designed by natural information to explain the prey selection of predators selection to maximize its net rate of food intake that feed on the two types of prey species (sessile (Krebs, 1977; Hughes, 1980). and mobile). Generalist predators have an important role in The biggest problem in evaluating the com­ the community structure: they stabilize prey position of prey in the natural environment neither populations and affect the diversity of their is that the observation of the predatory behavior communities through prey selection (Menge & (observed diet) nor always indicates the composition Sutherland, 1976; Alford, 1989; Kurzava & Morin, of natural prey (real diet). A reason for this 1998; Lambinet al., 2000). Few studies have discrepancy is the regularity of foraging behavior in quantitatively analyzed prey selection or prey the intertidal zones (Yamamoto, 2004). Although composition of generalist predators (Spiller & many predators have different foraging behavior Schoener, 1990; Wootton, 1997; Eisenberg et al., 2000). patterns between high tide and low tide, many of the Feeding strategies may also differ with studies were lead during low tide (Fairweather & relation to the number of prey items eaten. Dietary Underwood, 1983; McQuaid, 1985; Moran, 1985b; generalists eat wider ranges of prey than dietary Abe, 1989). Another reason is the difference in specialists (Curio, 1976). Specialization should be handling time in different types of prey, where those effective enough to achieve optimal hunting success that demand a bigger time are more frequently but at the same time it should not be so rigid as to observed (Peterson & Bradley, 1978; Fairweather & prevent the predator from changing from a particular Underwood, 1983; Abe, 1989). and originally preferred prey species when that The gastropod family Fasciolariidae is formed species becomes rare (Curio, 1976). by carnivorous species, usually preying on bivalves The food value of different food items can be and others gastropods (Fretter & Graham, 1962; compared by measuring their size, handling time Paine, 1963; Owen, 1966; Matthews-Cascon et al., (the time that a predator takes capturing, subduing, 1989; Meirelles & Matthews-Cascon, 2003). It is consuming, and digesting a prey) and / or caloric attributed for this family, as strategy of predation, content (Matthews-Cascon, 1997). the prey shell chipping, means by which the predator The diet type and variety of mechanisms that can reach the soft parts of the prey (Hughes, 1986). are used in the search of food presented by members Paine (1963) studied the alimentary preference of Gastropoda are amazing if compared with other and the predation rate of giganteus groups (Ankel, 1938; Graham, 1955; Owen, (Kiener, 1840) in Florida, determining that this 1966). They show all different types of alimentary species is a generalist predator, also preying habits: herbivores, deposit-feeders, suspension-fee­ of the same subfamily as hunteria (Perry, ders, scavengers and parasites (Hughes, 1986). The 1811) and tulipa (Weisbord, 1962). main structure that allows this extensive alimentary On the predation of Aurantilaria aurantiaca variation is the complex formed by the / (Lamarck, 1816) two studies have been conducted: buccal cavity (Owen, 1966). one by Schmitt (1994), that affirms its alimentary Some studies have been carried through preference in laboratory conditions for Fissurella evaluating aspects of behavior of gastropod preda­ rosea (Gmelin, 1791) and the process of predation tors using the optimal foraging theory (OFT) involves the braking of prey shell. The other Meirelles (Menge, 1978; Hughes & Dunkin, 1984a,b; Hughes & Matthews-Cascon (2003) analyzes the relation that & Drewett, 1985; McQuaid, 1985; Abe, 1989; exists between shell size and radula size in 14 species Burrows & Hughes, 1989; Duarte, 1990; Palmer, of marine prosobranchs with different types of diet. 1990; Richardson & Brown, 1990; Hughes et al., Aurantilaria aurantiaca showed no significant result 1992; Richardson & Brown, 1992; Hughes & for this relation, demonstrating that radula size does Burrows,1994; Etter, 1996; Brown, 1997; Meirelles & not interfere on the prey processing. Matthews-Cascon, 2003). In the present study, predatory behavior and However, certain foraging behaviors of prey preference of Aurantilaria aurantiaca in labo­ gastropod predators in the intertidal zone could not ratory conditions were investigated.

24 Arq. Ciên. Mar, Fortaleza, 2016, 49(2): 23 - 32 MATERIALS AND METHODS Eighteen adult animals of A. aurantiaca were collected manually, kept in plastic boxes with Field Studies constant aeration and transferred to the Laboratory of Marine Invertebrates of the Department of Biology During the year of 2005, monthly observations – Universidade Federal do Ceará (UFC). Also the of predatory activity of Aurantilaria aurantiaca (Figure possible prey species available for the experiment in 1) were made, during the low tides, at Pacheco Beach laboratory were collected. (3o 41’S; 38o 37’W), Ceará State, Northeast Brazil (Figure 2), to determine its possible preys. Laboratory Proceeding

Five specimens of A. aurantiaca were anes­ thetized with a saturated solution of seawater + freshwater (1:1) and magnesium chloride during 3 hours. The animals were measured with a vernier caliper to 0.1 mm of precision (shell length was considered the distance from the apex to the tip of the ) and had their stomach contents observed under optic micro­ scope and stereoscopic microscope. The 13 remaining specimens were kept indi­ vidually in 13 tanks of 5 liters with seawater from the study area, constant aeration, temperature of 28°C and 35 of salinity. These animals remained in Figure 1 - Adult individual of Aurantilaria aurantiaca from Pacheco a period of 7 days without food before the Beach – Ceará State, Northeast Brazil (Shell length: 90 mm). experiments. Prey samples for the experiments were kept separated by species in a 60 liters tank with seawater from the study area and in the same conditions of Aurantilaria aurantiaca tanks.

Prey Preference Experiment

Individuals of Aurantilaria aurantiaca were placed separately in 16 x 8 x 10 cm plastic boxes. Each A. aurantiaca was placed with one individual of each prey species. During this experiment the number of consumed prey was noted and eaten individuals were replaced. This experiment lasted for 2 months and was replicated 10 times. The mean number of individuals of each species consumed was calculated per each week of the experiment. Percentage of predators that recognized each species as a prey was calculated. Individuals of A. aurantiaca were placed separately in plastic boxes with 3 individuals of the same prey species and used as control group. Statistical tests were applied using program STATISTICA 7. Initially, data normality and its Figure 2 - Map indicating the sampling area at Pacheco Beach, averages were verified and then submitted to the Ceará State, Northeast Brazil. correlation test.

Arq. Ciên. Mar, Fortaleza, 2016, 49(2): 23 - 32 25 Handling Time Experiment Pisania pusio was found in cracks or under rocks, most of it being solitary individuals (Figure The handling time of predation was measured 3A). Tegula viridula and Stramonita brasiliensis were by placing 1 adult predator with 1 prey into separate observed inhabiting the same area and these containers and placing them in an 80 liters tank (total populations were always aggregated in large groups of 10 boxes and 10 predators) with seawater from the (Figure 3C and 3E). study area, constant aeration, temperature of 28°C The sampled specimens of Aurantilaria and 35 of salinity. Observations were made every 2 aurantiaca measured 66.48 ± 4.9 mm (n = 18), Pisania hours during 24 hours over 30 days period. This pusio measured 24.51 ± 1.23 mm (n = 160) and experiment was replicated 10 times for each prey Stramonita brasiliensis 33.42 ± 2.19 mm (n = 300) in species. The time interval from the first successful length. Tegula viridula measured 16.08 ± 0.89 mm (n = attack to the separation of the predator and empty 300), considering the shell length the distance from prey shell was recorded. the apex to the farthest point of the outer . The stomach content of Aurantilaria aurantiaca RESULTS showed no identifiable material.

Observations made in the study area have Prey Preference shown the presence of Aurantilaria aurantiaca only on beach rocks. Three gastropod species were seen Aurantilaria aurantiaca showed preference for being preyed upon by it: Pisania pusio (Linnaeus, Stramonita brasiliensis that consumed in 60 days the 1758) (Figure 3A and 3B), Tegula viridula (Gmelin, total of 97 individuals, in a rate of 1.6 preys per day. 1791) (Figure 3C and 3D) and Stramonita brasiliensis The statistical test showed that the average number (Linnaeus, 1767) (Figure 3E and 3F). of individuals of Stramonita brasiliensis consumed per week had a normal distribution, with significant increase during the experiment (p = 0.0008; r = 0.9050), mainly from the fifth week, varying from 1.14 preys in the first week to 3.14 preys in the eighth week (Figure 4 and 5A).

Figure 3 - Gastropods preyed by Aurantilaria auratiaca at Pacheco Beach, Ceará State, Northeast Brazil. A. Individuals of Pisania pusio. B. Ventral and dorsal view of P. pusio shell. C. Individuals of Tegula viridula. D. Ventral and dorsal view of T. viridula shell. E. Individuals of Stramonita brasiliensis. F. Ventral and dorsal view of S. brasiliensis shell.

26 Arq. Ciên. Mar, Fortaleza, 2016, 49(2): 23 - 32 The second most consumed prey was Pisania pusio, in a total of 53 individuals. The weekly average A of animals eaten did not have significant variation (normal distribution) (p = 0.7235; r = 0.1379) and the consumption rate was 0.88 prey per day. It was observed that in the second week the average number of consumed animals was higher than S. brasiliensis, occurring a high decreasing of these values until the fourth week, when no specimen of Pisania pusio was eaten (Figure 4 and 5B). Tegula viridula was the prey that reached the lower number of animals eaten during the expe­ riment, in a total of 25 individuals. The consumption B rate was 0.41 individuals per day and the weekly average of animals eaten was not statistically significant (normal distribution) (p = 0.2499; r= 0.4284), reaching the same value that Pisania pusio did in the end of the eighth week (0.57 prey eaten/ week) (Figure 4 and 5C). The percentage of individuals of Aurantilaria aurantiaca that recognized Stramonita brasiliensis as a prey during the 8 weeks had a significant increase during the experiment (p = 0.0007), varying 50% in the first week to 100% in the eighth week (Figure 6). C

Figure 5 - Variation of the mean number of prey eaten by Aurantilaria aurantiaca during a 60 day period experiment. A. Stramonita Figure 4 - Mean number of prey eaten by Aurantilaria aurantiaca brasiliensis (p=0,0008; r = 0,9050). B. Pisania pusio (p = 0,7235; r = during a 60 day period experiment (Error Bar = SD). 0,1379). C. Tegula viridula (p = 0,2499; r = 0,4284).

Figure 6 - Percentage of individuals (n = 10) of Aurantilaria aurantiaca that recognized each prey during a 60 days period.

Arq. Ciên. Mar, Fortaleza, 2016, 49(2): 23 - 32 27 Although Pisania pusio was recognized with the cephalic region in contact with the of the same percentage that Stramonita brasiliensis during prey shell. the two first weeks, it did not have significant weekly After this first contact, Aurantilaria aurantiaca variation (p = 0.4412) during experiment (Figure 6). used two ways of predation: (1) immediately Tegula viridula was the least consumed species by attacked the prey with its proboscis, placing it Aurantilaria aurantiaca, reaching values between between the aperture of the prey shell and the 10% and 30% of predators that recognized it as a , preventing the prey to retract to the prey. Pisania pusio also did not reach significant interior of the shell; (2) when the prey retracted variation of predator recognition during the before the introduction of predator proboscis, the experiment (p = 0.2661) (Figure 6). predator tried to suffocate it with the foot, covering It was observed that during the 60 days of all the area of the prey shell aperture (Figure 8). the experiment, the percentage of predators that The aperture of the shells of the 3 prey species did not feed in each week decreased significantly did not presented any type of breaking or damage (p = 0.0415) (Figure 6). after the predation (n = 100). Almost all soft parts of the prey were consumed, remaining only some parts Handling Time of the muscle of the foot on the operculum. The examined opercula did not show any type of scraped The handling time was shorter when Auran­ made by the radula (n = 100). tilaria aurantiaca preyed on Stramonita brasiliensis (2.5 ± Stramonita brasiliensis presented 3 types of 0.3 hrs, n = 161) (Table I) (Figure 7) than when it anti-predatory behavior: (1) it was the only species preyed on the two others species, Pisania pusio 4.83 ± of prey that reacted before the presence of the 1.8 hrs (n = 88) (Table I) (Figure 7) and Tegula viridula predator, adopting behavior of escape and search for 7.24 ± 3.1hrs (n = 46) (Table I) (Figure 7). All predators preyed on S. brasiliensis, Table I - Handling time of predation by Aurantilaria aurantiaca sometimes more than one prey per day. The amount on Pisania pusio, Tegula viridula and Stramonita brasiliensis in labo- of individuals of S. brasiliensis consumed per ratory conditions. predator during 30 days was 15.83 (Table I), P. pusio Pisania Tegula Stramonita Handling Time Exp. was 12.09 and T. viridula was 4.32 (Table I). pusio viridula brasiliensis

Predatory Behavior N. of observations 360 360 360 N. of replications 10 10 10 Total observations 3600 3600 3600 Aurantilaria aurantiaca has the same predatory Total prey 12,09 4,32 15,83 behavior when attacks the 3 preys used in this study. consummed/predator After the identification of the prey, the predator Mean handling time 4,83 ± 1,8 7,24 ± 3,1 2,5 ± 0,3 holds it firmly with the foot, trying to keep the (hours)

Figure 7 - Handling time of predation of Aurantilaria aurantiaca on Pisania pusio, Tegula viridula and Stramonita brasiliensis in laboratory conditions (Error bar = SD).

28 Arq. Ciên. Mar, Fortaleza, 2016, 49(2): 23 - 32 shelter. It crawled to the top of the predator shell in Induced defenses by the presence of the some observations, avoiding the predator searching; predator are a generalized phenomenon, especially (2) in the moment of the predator attack, some in marine shallow waters (Vermeij, 1987; Harvell, individuals of Stramonita brasiliensis extruded the 1990). An anti-predatory specific type in an only proboscis and counterattacking using the radula; (3) time and space can be a characteristic badly in the instant of the attack, it was possible to observe adaptative if applied to others, therefore, induced clearly the release of a liquid substance from the defenses would have to favor in cases where the prey, of yellowish tone that in contact with the predatory pressure varies in time and space, thus seawater became purple. This substance is very getting trustworthy strategies (Havel, 1987; Harvell, common in Thaididae (Nicol, 1964). 1990; Yamada et al., 1998). Tegula viridula was the less consumed prey, probably due to the long handling time associated with the small aperture of its shell. Probably the optimal foraging theory can explain the preference of prey by Aurantilaria aurantiaca, since that the anti-predatory behavior of Stramonita brasiliensis did not interfere with the prey choice and that, although the predation on Pisania pusio and Tegula viridula were not statistically signifi­ cant, the predator showed a generalist predatory behavior, consuming all 3 prey species. The preference experiment showed that the specimen number of Stramonita brasiliensis preyed in each week increased significantly, including the percentage of predators that recognized them as a prey. Probably, Aurantilaria aurantiaca showed a Figure 8 - Aurantilaria aurantiaca and its suffocating predatory process of ingestive conditioning (Wood, 1968). behavior when it tries to prey an individual of Stramonita brasiliensis. According to Wood (1968), ingestive condi­ tioning is a modification and/or reinforcement of DISCUSSION prey preferences in response to chemicals from prey that had been consumed recently. Ingestive condi­ The preference for Stramonita brasiliensis tioning may involve a training process (Hall et al., over Pisania pusio and Tegula viridula demonstrated 1982). For example, in birds this training involves by Aurantilaria aurantiaca may be due to the fact that the formation of a search image (Royama, 1970; S. brasiliensis requires a shorter handling time and Dawkins, 1971). In gastropods the process was the aperture of its shell is wider than that from the shown after the predator had many encounters with other preys. the prey (Murdoch, 1969) but it must be chemical Although S. brasiliensis was the only prey and not visual as in birds. that presented relatively aggressive anti-predatory The handling time presented for Stramonita behavior, it did not show much efficiency when brasiliensis demonstrated that the predator probably tried to escape from the predator. S. brasiliensis is a already has been in contact with the prey. The results moluscivore species as well as A. aurantiaca and indicate that until the second week of experiment of did not prey any of the other species used in the alimentary preference, attacks from A. aurantiaca experiment. over S. brasiliensis and Pisania pusio were the same, The vulnerability of the prey is higher when it but later, the preference for S. brasiliensis increased is under stress energy, due to allocation of the significantly. It decreased for P. pusio, reaching zero available energy for the anti-predatory behavior attack in the fourth week. (Caraco et al., 1980; Fitzgibbon, 1989; Bachman, 1993; The learning process in Aurantilaria aurantiaca Lima, 1998). In the preference experiment, the can clearly be seen when we observe its predation on presence of A. aurantiaca probably inhibited the Tegula viridula, which presented in the first week of predatory behavior and stimulating the anti- experiment the handling time of 12 hours. In the end predatory behavior in S. brasiliensis, probably of the experiment this time decreased to 4 hours i.e. the making it more vulnerable. predator tends to increase its efficiency at the moment

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